BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair

Genes and Development

Volumn 25, Issue 4, 2011, Pages 350-362

  Nimonkar, Amitabh V ^a   Genschel, Jochen ^b   Kinoshita, Eri ^c   Polaczek, Piotr ^d   Campbell, Judith L ^d   Wyman, Claire ^c   Modrich, Paul ^b   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

BLM helicase; DNA break repair; DNA end resection; DNA2 nuclease; EXO1 nuclease; Homologous recombination

Indexed keywords

ADENOSINE TRIPHOSPHATE; BLOOM SYNDROME HELICASE; DNA2 HELICASE; EXONUCLEASE; EXONUCLEASE 1; HELICASE; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN; REPLICATION FACTOR A; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; DNA DENATURATION; DNA END RESECTION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA BREAKS, SINGLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; HUMANS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN BINDING; RECQ HELICASES; REPLICATION PROTEIN A;

EID: 79951688343     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.2003811     Document Type: Article

References (60)

1. Bae SH, Bae KH, Kim JA, Seo YS. 2001. RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412: 456-461.
2. Brosh RM Jr, Li JL, Kenny MK, Karow JK, Cooper MP, Kureekattil RP, Hickson ID, Bohr VA. 2000. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J Biol Chem 275: 23500-23508. (Pubitemid 30624631)
3. Budd ME, Campbell JL. 2009. Interplay of Mre11 nuclease with Dna2 plus Sgs1 in Rad51-dependent recombinational repair. PLoS ONE 4: e4267. doi: 10.1371/journal/pone.0004267.
4. Budd ME, Choe W, Campbell JL. 2000. The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. J BiolChem275: 16518-16529. (Pubitemid 30398875)
5. Bugreev DV, Yu X, Egelman EH, Mazin AV. 2007. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev 21: 3085-3094. (Pubitemid 350223526)
6. Buis J, Wu Y, Deng Y, Leddon J, Westfield G, Eckersdorff M, Sekiguchi JM, Chang S, Ferguson DO. 2008. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135: 85-96.
7. Cejka P, Kowalczykowski SC. 2010. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds Holliday junctions. J Biol Chem 285: 8290-8301.
8. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, Campbell JL, Kowalczykowski SC. 2010a. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467: 112-116.
9. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. 2010b. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol 17: 1377-1382.
10. Chester N, Kuo F, Kozak C, O'Hara CD, Leder P. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev 12: 3382-3393. (Pubitemid 28520986)
11. Chiolo I, Carotenuto W, Maffioletti G, Petrini JH, Foiani M, Liberi G. 2005. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol Cell Biol 25: 5738-5751. (Pubitemid 40853606)
12. Chu WK, Hickson ID. 2009. RecQ helicases: Multifunctional genome caretakers. Nat Rev Cancer 9: 644-654.
13. Dillingham MS, Kowalczykowski SC. 2008. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol Mol Biol Rev 72: 642-671.
14. Duxin JP, Dao B, Martinsson P, Rajala N, Guittat L, Campbell JL, Spelbrink JN, Stewart SA. 2009. Human dna2 is a nuclear and mitochondrial DNA maintenance protein. Mol Cell Biol 29: 4274-4282.
15. Dzantiev L, Constantin N, Genschel J, Iyer RR, Burgers PM, Modrich P. 2004. A defined human system that supports bidirectional mismatch-provoked excision. Mol Cell 15: 31-41. (Pubitemid 38850217)
16. Eid W, Steger M, El-Shemerly M, Ferretti LP, Pena-Diaz J, Konig C, Valtorta E, Sartori AA, Ferrari S. 2010. DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep 11: 962-968.
17. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: A potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398. (Pubitemid 24373588)
18. Garcia PL, Liu Y, Jiricny J, West SC, Janscak P. 2004. Human RECQ5β, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J 23: 2882-2891. (Pubitemid 39013560)
19. Genschel J, Modrich P. 2003. Mechanism of 5′-directed excision in human mismatch repair. Mol Cell 12: 1077-1086. (Pubitemid 37487919)
20. German J. 1993. Bloom syndrome: A mendelian prototype of somatic mutational disease. Medicine 72: 393-406.
21. Gravel S, Chapman JR, Magill C, Jackson SP. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 22: 2767-2772.
22. Handa N, Morimatsu K, Lovett ST, Kowalczykowski SC. 2009. Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev 23: 1234-1245.
23. Harmon FG, Kowalczykowski SC. 1998. RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev 12: 1134-1144. (Pubitemid 28194049)
24. Harmon FG, Kowalczykowski SC. 2001. Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J Biol Chem 276: 232-243. (Pubitemid 32050312)
25. Hartsuiker E, Neale MJ, Carr AM. 2009. Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) in the removal of covalently bound topoisomerase I and II from DNA. Mol Cell 33: 117-123.
26. Hopkins BB, Paull TT. 2008. The P. furiosus Mre11/Rad50 complex promotes 5′ strand resection at a DNA double-strand break. Cell 135: 250-260.
27. Imamura O, Campbell JL. 2003. The human Bloom syndrome gene suppresses the DNA replication and repair defects of yeast dna2 mutants. Proc Natl Acad Sci 100: 8193-8198. (Pubitemid 36842521)
28. Inbar O, Kupiec M. 1999. Homology search and choice of homologous partner during mitotic recombination. Mol Cell Biol 19: 4134-4142. (Pubitemid 29241987)
29. Kim JH, Kim HD, Ryu GH, Kim DH, Hurwitz J, Seo YS. 2006. Isolation of human Dna2 endonuclease and characterization of its enzymatic properties. Nucleic Acids Res 34: 1854-1864.
30. Lee BI, Wilson DM III. 1999. The RAD2 domain of human exonuclease 1 exhibits 5′ to 3′ exonuclease and flap structure-specific endonuclease activities. J Biol Chem 274: 37763-37769.
31. Liao S, Toczylowski T, Yan H. 2008. Identification of the Xenopus DNA2 protein as a major nuclease for the 5′ → 3′ strandspecific processing of DNA ends. Nucleic Acids Res 36: 6091-6100.
32. Llorente B, Symington LS. 2004. The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol Cell Biol 24: 9682-9694. (Pubitemid 39391702)
33. Lovett ST, Kolodner RD. 1989. Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc Natl Acad Sci 86: 2627-2631. (Pubitemid 19112600)
34. Luo G, Santoro IM, McDaniel LD, Nishijima I, Mills M, Youssoufian H, Vogel H, Schultz RA, Bradley A. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat Genet 26: 424-429.
35. Masuda-Sasa T, Imamura O, Campbell JL. 2006. Biochemical analysis of human Dna2. Nucleic Acids Res 34: 1865-1875.
36. Masuda-Sasa T, Polaczek P, Peng XP, Chen L, Campbell JL. 2008. Processing of G4 DNA by Dna2 helicase/nuclease and replication protein A (RPA) provides insights into the mechanism of Dna2/RPA substrate recognition. J Biol Chem 283: 24359-24373.
37. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774.
38. Mimitou EP, Symington LS. 2010. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J 29: 3358-3369.
39. Mohaghegh P, Karow JK, Brosh RM Jr, Bohr VA, Hickson ID. 2001. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 29: 2843-2849. (Pubitemid 32685049)
40. Moreau S, Ferguson JR, Symington LS. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19: 556-566. (Pubitemid 29018457)
41. Myers RS, Stahl MM, Stahl FW. 1995. Chi recombination activity in phage λ decays as a function of genetic distance. Genetics 141: 805-812. (Pubitemid 3003907)
42. Nicolette ML, Lee K, Guo Z, Rani M, Chow JM, Lee SE, Paull TT. 2010. Mre11-Rad50-Xrs2 and Sae2 promote 5′ strand resection of DNA double-strand breaks. Nat Struct Mol Biol 17: 1478-1485.
43. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC. 2008. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci 105: 16906-16911.
44. Niu H, Chung WH, Zhu Z, Kwon Y, Zhao W, Chi P, Prakash R, Seong C, Liu D, Lu L, et al. 2010. Mechanism of the ATP-dependent DNA end resection machinery from Saccharomyces cerevisiae. Nature 467: 108-111.
45. Paull TT, Gellert M. 1998. The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol Cell 1: 969-979. (Pubitemid 128379258)
46. Perrin A, Buckle M, Dujon B. 1993. Asymmetrical recognition and activity of the I-SceI endonuclease on its site and on intron-exon junctions. EMBO J 12: 2939-2947. (Pubitemid 23218344)
47. Rossi ML, Ghosh AK, Kulikowicz T, Croteau DL, Bohr VA. 2010. Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding. DNA Repair (Amst) 9: 796-804.
48. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450: 509-514. (Pubitemid 350190253)
49. Schmutte C, Marinescu RC, Sadoff MM, Guerrette S, Overhauser J, Fishel R. 1998. Human exonuclease I interacts with the mismatch repair protein hMSH2. Cancer Res 58: 4537-4542.
50. Shim EY, Chung WH, Nicolette ML, Zhang Y, Davis M, Zhu Z, Paull TT, Ira G, Lee SE. 2010. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J 29: 3370-3380.
51. Stracker TH, Theunissen JW, Morales M, Petrini JH. 2004. The Mre11 complex and the metabolism of chromosome breaks: The importance of communicating and holding things together. DNA Repair (Amst) 3: 845-854. (Pubitemid 38997926)
52. Szankasi P, Smith GR. 1992. A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J Biol Chem 267: 3014-3023.
53. Tishkoff DX, Amin NS, Viars CS, Arden KC, Kolodner RD. 1998. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease implicated in mismatch repair and recombination. Cancer Res 58: 5027-5031. (Pubitemid 28521153)
54. Wawrousek KE, Fortini BK, Polaczek P, Chen L, Liu Q, Dunphy WG, Campbell JL. 2010. Xenopus DNA2 is a helicase/nuclease that is found in complexes with replication proteins And-1/Ctf4 and Mcm10 and DSB response proteins Nbs1 and ATM. Cell Cycle 9: 1156-1166.
55. White CI, Haber JE. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J 9: 663-673.
56. Wilson DM III, Carney JP, Coleman MA, Adamson AW, Christensen M, Lamerdin JE. 1998. Hex1: A new human Rad2 nuclease family member with homology to yeast exonuclease 1. Nucleic Acids Res 26: 3762-3768. (Pubitemid 28367983)
57. Wu L, Hickson ID. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874. (Pubitemid 38056876)
58. Wu L, Davies SL, Levitt NC, Hickson ID. 2001. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J Biol Chem 276: 19375-19381.
59. Wyman C, Kanaar R. 2006. DNA double-strand break repair: All's well that ends well. Annu Rev Genet 40: 363-383. (Pubitemid 44956790)
60. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994.